Molecular Biology Reports

, Volume 40, Issue 4, pp 3363–3371 | Cite as

Molecular analysis of the bacterial microbiome in the forestomach fluid from the dromedary camel (Camelus dromedarius)

  • Vaibhav D. Bhatt
  • Suchitra S. Dande
  • Nitin V. Patil
  • Chaitanya G. Joshi
Article

Abstract

Rumen microorganisms play an important role in ruminant digestion and absorption of nutrients and have great potential applications in the field of rumen adjusting, food fermentation and biomass utilization etc. In order to investigate the composition of microorganisms in the rumen of camel (Camelus dromedarius), this study delves in the microbial diversity by culture-independent approach. It includes comparison of rumen samples investigated in the present study to other currently available metagenomes to reveal potential differences in rumen microbial systems. Pyrosequencing based metagenomics was applied to analyze phylogenetic and metabolic profiles by MG-RAST, a web based tool. Pyrosequencing of camel rumen sample yielded 8,979,755 nucleotides assembled to 41,905 sequence reads with an average read length of 214 nucleotides. Taxonomic analysis of metagenomic reads indicated Bacteroidetes (55.5 %), Firmicutes (22.7 %) and Proteobacteria (9.2 %) phyla as predominant camel rumen taxa. At a finer phylogenetic resolution, Bacteroides species dominated the camel rumen metagenome. Functional analysis revealed that clustering-based subsystem and carbohydrate metabolism were the most abundant SEED subsystem representing 17 and 13 % of camel metagenome, respectively. A high taxonomic and functional similarity of camel rumen was found with the cow metagenome which is not surprising given the fact that both are mammalian herbivores with similar digestive tract structures and functions. Combined pyrosequencing approach and subsystems-based annotations available in the SEED database allowed us access to understand the metabolic potential of these microbiomes. Altogether, these data suggest that agricultural and animal husbandry practices can impose significant selective pressures on the rumen microbiota regardless of rumen type. The present study provides a baseline for understanding the complexity of camel rumen microbial ecology while also highlighting striking similarities and differences when compared to other animal gastrointestinal environments.

Keywords

Metagenomes Pyrosequencing MG-RAST SEED subsystem Bacteroides and camel 

Abbreviations

MG-RAST

Metagenome rapid annotation using subsystem technology

GS-FLX

Genome sequencer flexible

SSU

Small subunit

COG

Clusters of orthologous groups

KO

KEGG orthology

NOG

Non-supervised orthologous group

Supplementary material

11033_2012_2411_MOESM1_ESM.txt (1.1 mb)
Supplementary file 1: Sequences of predominant bacterial species found in the present study. (TXT 1137 kb)

References

  1. 1.
    Ahmad S, Yaqoob M, Hashmi N, Ahmad S, Zaman MA, Tariq M (2010) Economic importance of camel: unique alternative under crisis. Pak Vet J 30:1–7Google Scholar
  2. 2.
    Van Soest PJ (1994) Nutritional ecology of the ruminant, 2nd edn. Cornell University Press, IthacaGoogle Scholar
  3. 3.
    Samsudin AA, Paul NE, Andre-Denis GW, Rafat AJ (2011) Molecular diversity of the foregut bacteria community in the dromedary camel (Camelus dromedarius). Environ Microbiol 13:3024–3035PubMedCrossRefGoogle Scholar
  4. 4.
    Krause DO, Russell JB (1996) How many ruminal bacteria are there? J Dairy Sci 79:1467–1475PubMedCrossRefGoogle Scholar
  5. 5.
    Shin EC, Choi BR, Lim WJ, Hong SY, An CL et al (2004) Phylogenetic analysis of archaea in three fractions of cow rumen based on the 16S rDNA sequence. Anaerobe 10:313–319PubMedCrossRefGoogle Scholar
  6. 6.
    Sylvester JT, Karnati SK, Yu Z, Morrison M, Firkins JL (2004) Development of an assay to quantify rumen ciliate protozoal biomass in cows using real-time PCR. J Nutr 134:3378–3384PubMedGoogle Scholar
  7. 7.
    Kocherginskaya SA, Aminov RI, White BA (2001) Analysis of the rumen bacterial diversity under two different diet conditions using denaturing gradient gel electrophoresis, random sequencing, and statistical ecology approaches. Anaerobe 7:119–134CrossRefGoogle Scholar
  8. 8.
    Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mole Biol Rev 68:669–685CrossRefGoogle Scholar
  9. 9.
    Edwards RA, Rodriguez BB, Wegley L, Haynes M, Breitbart M et al (2006) Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics 7:57–69PubMedCrossRefGoogle Scholar
  10. 10.
    Margulies M, Egholm M, Altman WE, Attiya S, Bader JS et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedGoogle Scholar
  11. 11.
    Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM et al (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120PubMedCrossRefGoogle Scholar
  12. 12.
    Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK et al (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290PubMedGoogle Scholar
  13. 13.
    Yu Z, Yu M, Morrison M (2006) Improved serial analysis of V1 ribosomalsequence tags (SARST-V1) provides a rapid, comprehensive, sequence-basedcharacterization of bacterial diversity and community composition. Environ Microbiol 8:603–611PubMedCrossRefGoogle Scholar
  14. 14.
    Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM et al (2008) The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386PubMedCrossRefGoogle Scholar
  15. 15.
    Madigan M, Martinko J (2005) Brock biology of microorganisms, 11th edn. Prentice Hall, Upper Saddle RiverGoogle Scholar
  16. 16.
    Dorland WAN (2003) Dorland’s illustrated medical dictionary, 30th edn. W. B. Saunders, PhiladelphiaGoogle Scholar
  17. 17.
    Wexler HM (2007) Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 20:593–621PubMedCrossRefGoogle Scholar
  18. 18.
    Xu J, Mahowald A, Ley E, Lozupone A, Hamady M, Martens C, Henrissat B, Coutinho M et al (2007) Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 5:156CrossRefGoogle Scholar
  19. 19.
    Martens EC, Chiang HC, Gordon JI (2008) Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 13:447–457CrossRefGoogle Scholar
  20. 20.
    Bernhard AE, Katharine GF (2000) A PCR assay to discriminate human and ruminant feces on the basis of host differences in bacteroides-prevotella genes encoding 16S rRNA. Appl Environ Microbiol 66:4571–4574PubMedCrossRefGoogle Scholar
  21. 21.
    Kreader CA (1998) Persistence of PCR-detectable bacteroides distasonis from human feces in river water. Appl Environ Microbiol 64:4103–4105PubMedGoogle Scholar
  22. 22.
    Shipman JA, Cho HK, Siegel HA, Salyers AA (1999) Physiological characterization of SusG, an outer membrane protein essential for starch utilization by Bacteroides thetaiotaomicron. J Bacteriol 181:7206–7211PubMedGoogle Scholar
  23. 23.
    Jian Xu, Gordon JI (2003) Honor thy symbionts. Proc Natl Acad Sci USA 100:10452–10459CrossRefGoogle Scholar
  24. 24.
    Miron J, Ben-Ghedalia D, Morrison M (2001) Invited review: adhesion mechanisms of rumen cellulolytic bacteria. J Dairy Sci 84:1294–1309PubMedCrossRefGoogle Scholar
  25. 25.
    Sung HG, Kobayashi Y, Chang J, Ha A, Hwang H, Ha JK (2007) Low ruminal pH reduces dietary fiber digestion via reduced microbial attachment. Asian-Aust J Anim Sci 20:200–207Google Scholar
  26. 26.
    Russell JB, Rychlik JL (2001) Factors that alter rumen microbial ecology. Science 292:1119–1122PubMedCrossRefGoogle Scholar
  27. 27.
    Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651PubMedCrossRefGoogle Scholar
  28. 28.
    Leser TD, Amenuvor JZ, Jensen TK, Lindecrona RH, Boye M, Moller K (2002) Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68:673–690PubMedCrossRefGoogle Scholar
  29. 29.
    Qu A, Brulc JM, Wilson MK, Law BF, Theoret JR et al (2008) Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS ONE 3:2945CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Vaibhav D. Bhatt
    • 1
  • Suchitra S. Dande
    • 2
  • Nitin V. Patil
    • 2
  • Chaitanya G. Joshi
    • 1
  1. 1.Department of Animal BiotechnologyCollege of Veterinary Science and A. H., Anand Agricultural UniversityAnandIndia
  2. 2.National Research Centre on CamelBikanerIndia

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